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Head and Neck Imaging |
1 From the Department of Radiology, Johns Hopkins University School of Medicine, 600 N Wolfe St, Baltimore, MD 21287 (D.A.B.); Department of Radiology, Cleveland Clinic, Ohio (A.E.S.); Department of Radiology, William Beaumont Hospital, Royal Oak, Mich (K.G.B.); Department of Radiology, University of Wisconsin, Madison (T.M.G.); Department of Radiology, Hospital of the University of Pennsylvania, Philadelphia (R.A.B.); Department of Radiology, Fletcher Allen Health Care, University of Vermont, Burlington (R.D.); Mallinckrodt Institute of Radiology, Washington University Medical Center, St Louis, Mo (E.S.M.); Mallinckrodt, St Louis, Mo (J.A.P.); and EPIX Medical, Cambridge, Mass (E.K.Y.). From the 1999 RSNA scientific assembly. Received May 19, 2000; revision requested July 12; revision received August 3; accepted September 12. D.A.B., A.E.S., K.G.B., T.M.G., R.A.B., R.D., and E.S.M. supported by grants from EPIX Medical and Mallinckrodt. Address correspondence to D.A.B. (e-mail: dbluemke@rad.jhu.edu).
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODS RESULTS DISCUSSIONREFERENCES |
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MATERIALS AND METHODS: Fifty carotid arteries in 26 patients were imaged with three-dimensional spoiled gradient-recalled-echo magnetic resonance (MR) angiography at 5 and 50 minutes after injection of MS-325. MS-325 was administered intravenously as a single dose of 0.01, 0.03, or 0.05 mmol per kilogram of body weight as determined with a dose randomization scheme for four, nine, and 13 patients, respectively. Safety, including clinical laboratory changes and electrocardiographic monitoring, was assessed until approximately 3 days after injection. Conventional contrast agent–enhanced angiography was used as the standard of reference. Independent readers blinded to the dose interpreted the MR angiographic and conventional images. Images were assessed for location and extent of carotid arterial stenosis.
RESULTS: There were no severe or serious adverse events. For the determination of clinically significant stenosis (>70%) on the 5-minute images, sensitivity, specificity, and accuracy (P = .07, three-way comparison) were 100%, 100%, and 100%; 63%, 100%, and 88%; and 40%, 75%, and 55% at 0.01, 0.03, and 0.05 mmol/kg, respectively. Sensitivity and specificity for images at 50 minutes after MS-325 administration showed the same trends as the 5-minute images.
CONCLUSION: Overall accuracy for MS-325–enhanced carotid MR angiography performed during steady-state conditions of circulating contrast agent approximately 5 minutes after injection was high (88%–100%) at 0.03 and 0.01 mmol/kg. MS-325 was well tolerated at all evaluated doses.
Index terms: Carotid arteries, MR, 904.12942, 904.12943 • Carotid arteries, stenosis or obstruction, 904.721 • Contrast media, experimental studies, 904.12942, 904.12943 • Magnetic resonance (MR), contrast media, 904.12942, 904.12943 • Magnetic resonance (MR), vascular studies, 904.12942, 904.12943
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTS DISCUSSIONREFERENCES |
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MS-325 is an investigational intravascular MR imaging contrast agent that binds strongly but reversibly to human serum albumin in the plasma (8,9). Because of albumin binding, MS-325 exhibits prolonged plasma elimination half-life and increased relaxivity. These properties may be particularly useful for contrast-enhanced 3D MR angiography. With prolonged T1 shortening of blood (6,10), MR angiogram resolution could be improved, since a longer imaging window is available after a single injection. Atherosclerotic disease frequently affects multiple vascular beds; an intravascular contrast agent could be useful to study several vascular territories. Finally, the requirement for high-performance-gradient systems potentially may be reduced with an intravascular contrast agent, thus widening the availability of MR angiography.
To our knowledge, the use of an intravascular contrast agent for carotid arterial imaging has not previously been evaluated specifically in humans. The purpose of this phase II multicenter study was to evaluate the safety and efficacy of MS-325 in patients suspected of having carotid arterial disease.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTS DISCUSSIONREFERENCES |
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Exclusion criteria included contraindication to MR imaging (eg, pacemaker, aneurysm clip); allergy to iodinated contrast agents; prior interventional procedure in the target vessel; endarterectomy or angioplasty within 14 days prior to MS-325 administration; known serum creatinine levels greater than 1.5 mg/dL (132.6 µmol/L); or clinical evidence of severe renal impairment. Patients with renal failure were excluded for safety reasons, because at the time of the study the effect of MS-325 on renal function had not been fully evaluated. Twenty-six patients (16 men, 10 women; age range, 42–81 years; mean age, 66.3 years) were enrolled from June 27, 1997, to March 10, 1998.
MS-325 Dose
Patients were placed randomly into one of three MS-325 dose groups. The dose coordinator at each of the study centers’ pharmacies contacted a central randomization center to randomly place each patient in a group receiving a dose of 0.01, 0.03, or 0.05 mmol of MS-325 per kilogram of body weight. The randomization scheme was designed to obtain a higher proportion of patients at the higher dose levels on the basis of results of the phase I study, which indicated increased efficacy at the higher dose levels (10). Table 1 shows the dose scheme.
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Injection of contrast agent and safety data were monitored in all patients in the phase II protocol. A brief medical history was obtained and physical examination was performed prior to administration of contrast agent. Vital signs (blood pressure, pulse, temperature, and respiratory rate) and electrocardiograms were obtained and clinical laboratory evaluations (including hematologic evaluation and coagulation factor levels; serum chemistry; urinalysis; and prothrombin time, partial thromboplastin time, and direct and indirect bilirubin levels) were performed prior to and following injection of contrast agent until 72–96 hours after injection. In addition, adverse events and concomitant medications were continuously recorded throughout the study period until 72–96 hours after injection of contrast agent. Adverse events were rated by the principal investigator at each site as follows: mild, experience is minor and does not cause substantial discomfort to the patient or change in activities of daily living; moderate, experience is of low-level inconvenience or concern to the patient and the patient is able to continue with activities of daily living; or severe, experience substantially interferes with activities of daily living.
MR Angiography
After MS-325 administration, each patient underwent MR angiography beginning at 5 minutes after the start of the injection and again at 50 minutes after injection. A subset of patients (five of 26) also underwent imaging immediately after MS-325 injection ("0-minute" images). This subset of images was analyzed for only SNR and contrast-to-noise ratio (CNR).
Contrast-enhanced MR angiography was performed by using a 3D spoiled gradient-echo sequence with 33/5 (repetition time msec/echo time msec) or less; flip angle, 15°–40°; field of view, 24 cm or less; 512 frequency encoding; and 192–394 phase-encoding steps. Since the dose of contrast agent was administered in a blinded fashion over a fivefold range of doses, the flip angle could not be optimized for each patient. Also, variation in pulse sequence was due to variation in MR imager performance at the seven participating institutions.
Imaging was performed with 1.5-T MR equipment (five Horizon imagers, GE Medical Systems, Milwaukee, Wis and three Vision imagers, Siemens, Erlangen, Germany). Parameters were, however, adjusted to image both carotid arteries 5–15 minutes after injection of contrast agent (5-minute images) and 50–60 minutes after injection of contrast agent (50-minute images). Images of the right and left carotid arteries were acquired with separate sagittal 3D slabs by using a section thickness of 1 mm or less and in-plane resolution of 0.7 x 0.9 mm or less. The mean imaging duration was 4 minutes 20 seconds for each carotid artery. All imaging was performed by using chemical shift spectrally selective fat suppression.
Conventional Angiography
Contrast-enhanced conventional angiography was performed according to institutional standards. Bilateral contrast-enhanced conventional angiography was performed in two orientations 90° apart by using a common carotid arterial injection and an image intensifier matrix of at least 512 x 512. Conventional angiography was performed between 72 hours and 30 days (inclusive) prior to MS-325 administration, or between 72 hours and 30 days (inclusive) after MS-325 administration. Conventional angiography performed within 6 days of MS-325 administration was performed by using nonionic contrast agents.
Image Interpretation
Each MR angiographic image was read by a single reader blinded to the dose, and a second independent reader blinded to the dose read all conventional angiograms. The readers were well versed in the reading of MR angiograms and conventional angiograms, respectively, and routinely read these types of images in their clinical practices. Each image of the carotid artery (right or left) was randomized within the patient population and presented to the reader separately. The readers had no knowledge of any patient information when reading the images.
The reader determined whether an image was technically satisfactory for determining the percentage of diameter stenosis (uninterpretable vs interpretable). If an image was not diagnostic (not technically satisfactory), it was rated as uninterpretable. Reasons included patient movement, improper position of the image acquisition volume, susceptibility (metal) artifact, inadequate vessel contrast, or other artifacts. If the image was determined to be uninterpretable, it was not subsequently analyzed and was not considered a false-positive finding. Images that were deemed interpretable were analyzed for degree of stenosis and overall image quality. Image quality was assessed subjectively on a five-point scale by the reader but was condensed for ease of presentation as follows: below average, which includes images rated poor or below average; average; or above average, which includes images rated above average or excellent.
MR image data were interpreted by using a maximum intensity projection (MIP) rotation series generated along a predetermined axis. Multiplanar reformatted image sets were generated in the transverse plane and in planes parallel and orthogonal to the vessel of interest. The MR angiography reader was supplied with source MIP and multiplanar reformatted images. The reader graded stenosis by using digital calipers.
For the conventional angiographic studies, stenosis grading was determined on the basis of digital imaging data. The conventional angiography reader measured vessel diameter for stenosis grading by using a calibrated magnifying glass. The conventional angiogram was used as the standard of reference in this trial.
Carotid arterial stenosis was measured at both conventional and MR angiography as a percentage of the diameter, on the basis of criteria established by the North American Symptomatic Carotid Endarterectomy Trial (11).
The disease state (clinically significant or not clinically significant) of the most severe stenoses was determined for both MR angiography and conventional angiography. A stenosis was defined as clinically significant if the percentage of diameter stenosis was greater than 70% (12). In addition, the degree of stenosis was categorized as follows: category 1, 0%–29% diameter stenosis; category 2, 30%–49% diameter stenosis; category 3, 50%–69% diameter stenosis; category 4, 70%–99% diameter stenosis; and category 5, occluded.
SNR was calculated for MR angiographic images by measuring the signal intensity of a homogeneous circular region of interest (ROI) over the common carotid artery, away from areas of stenosis. The ROI was positioned by an experienced data technologist with the supervision of a radiologist (E.K.Y.). The ROI size averaged 25.9 mm2, and the background averaged 280.1 mm2. CNR was calculated similarly by measuring the signal intensity of a homogeneous circular ROI over the sternocleidomastoid muscle with a mean ROI of 95.5 mm2. The background ROI was chosen anterior to the neck, and had a mean size of 280.1 mm2. The signal intensity of adjacent skeletal muscle in the neck was measured by carefully excluding vessels from the ROI. The SD of the background was measured by using an ROI placed over voxels containing air outside the neck. SNR was calculated as follows: carotid arterial signal intensity/SD of the background signal intensity. CNR was calculated as follows: (carotid arterial signal intensity - muscle signal intensity)/SD of background signal intensity. CNR and SNR data were calculated for 0-, 5-, and 50-minute images for the right carotid artery.
Volume-rendered images were assessed by two observers who were blinded to the dose of contrast agent; the observers were independent of the readers blinded to the dose, who interpreted the efficacy end points. The observers independently rated the depiction of the carotid arteries viewed from a sagittal targeted MIP image. The rated landmarks were the carotid arterial bifurcation and the proximal 2 cm of the internal and external carotid artery. A score of 1 indicated none of the landmarks could be identified because of overlap with the adjacent jugular vein, 2 indicated one landmark was depicted, 3 indicated two of the three landmarks were identified, and 4 indicated all landmarks were identified. Scoring was performed in 29 arteries that were imaged with the identical protocol at one institution; 30 arteries were available, but one was occluded. A single observer also performed quantitative volume-rendering measurements in 30 arterial segments to assess the degree of carotid arterial stenosis. Carotid arterial stenosis was measured with a digital caliper by using 50% opacity settings (13).
Statistical Methods
The primary end points of the study were the sensitivity, specificity, and overall accuracy for the 5- and 50-minute MR angiograms. Sensitivity was defined as the percentage of clinically significant stenoses correctly identified on the MR angiograms. Specificity was defined as the percentage of MR angiograms correctly identified as showing a lack of clinically significant stenosis. The conventional angiogram was the standard of reference in all cases. Accuracy was defined as the percentage of correct diagnoses (true-positive and true-negative diagnoses). Dose groups were compared by performing the Fisher exact test (14,15).
All analyses were performed by using commercially available software (SAS version 6; SAS Institute, Cary, NC). Statistical results were defined as significant for a P value of .05. Statistical results were defined as demonstrating a trend if the probability of obtaining the results by chance was greater than 0.05 and less than or equal to 0.10. All tests were two-tailed unless specified. Results for the left and right carotid arteries for each patient potentially showed within-patient correlation. To eliminate this effect, sensitivity, specificity, and accuracy were calculated for each side separately and then averaged. One-way analysis of variance, or ANOVA, results of mean SNR and mean CNR were analyzed.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTS DISCUSSIONREFERENCES |
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Images Obtained 5 Minutes after MS-325 Administration
There was good agreement between MR angiograms obtained 5 minutes after MS-325 administration and conventional angiograms for the determination of disease state (clinically significant vs not clinically significant) (Table 2). Sensitivity was 40%–100%, specificity was 75%–100%, and accuracy was 55%– 100%. A negative dose response was present; sensitivity, specificity, and accuracy decreased with increasing dose. Dose comparisons between the 0.01 and 0.05 mmol/kg dose groups and the 0.03 and 0.05 mmol/kg dose groups neared statistical significance (P = .083 and P = .088, respectively) (Table 2). The interpretability of the 5-minute images showed a dose response. Images were considered uninterpretable for one (12%) of eight, two (11%) of 18, and one (4%) of 24 MR angiograms at 0.01, 0.03, and 0.05 mmol/kg doses, respectively. Since flip angle may affect image quality, we evaluated the flip angle used as a function of MS-325 dose. The mean flip angles used were 28.8° (range, 25°–30°) for 0.01 mmol/kg, 27.5° (range, 25°–30°) for 0.03 mmol/kg, and 28.2° (range, 25°–40°) for 0.05 mmol/kg.
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Images Obtained 50 Minutes after MS-325 Administration
For images obtained beginning 50 minutes after MS-325 administration, there was again good correlation with conventional angiography for the disease state (Table 3). However, no clear dose response was noted, and there was no statistical difference in the comparison of the subgroups (Table 3). The overall ranges of sensitivities, specificities, and accuracies for each dose group were similar to those of the 5-minute images. As with the 5-minute images, a greater percentage of images obtained at the 0.01 mmol/kg dose were not interpretable (Table 3), compared with those obtained at the higher doses. For determining the degree of stenosis, overall agreement with the conventional angiogram increased with increasing dose (Table 3), but these results were not statistically significant when comparing dose groups. However, overall accuracies were lower when comparing the 50-minute to the 5-minute results (Table 2 vs Table 3).
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MIP Images and Volume Rendering
In three (10%) of 29 of the 5-minute MR angiograms, the carotid artery could not be separately identified from the internal jugular vein owing to overlap on the targeted sagittal MIP images (overlap score, 1). In seven (24%) of 29 cases, the overlap score was 2; in seven (24%) of 29 cases, the score was 3. In 12 (41%) of 29 cases, the carotid arterial depiction was rated as "4," indicating adequate artery-vein separation on MIP images. The two observers completely agreed in 21 (72%) of 29 cases. In the remaining eight (28%) cases, agreement was within one class of the arterial depiction score.
Interactive volume rendering was performed in a subset of studies to improve artery-vein separation. Carotid arterial stenosis assessed by using volume rendering was compared with that assessed with conventional angiography (Table 5). Overall, there was 90% agreement (27 of 30 cases) between the two methods. Errors in volume rendering were thought to be due to calcification in one case, which resulted in overestimation of the degree of stenosis and artery-vein overlap. The technical reasons for discrepancy were not apparent in the third case.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTS DISCUSSIONREFERENCES |
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In this study, we have demonstrated the preliminary efficacy of MS-325 for imaging the carotid arteries. Overall accuracy for MS-325–enhanced carotid MR angiography performed during steady-state conditions of circulating contrast agent approximately 5 minutes after injection was high (88%–100%) at 0.03 and 0.01 mmol/kg. These results showed marginal statistical significance and are comparable with accuracy for carotid MR angiography performed by using nonenhanced (17,18) and contrast-enhanced MR techniques with extracellular contrast agents (19,20). Accuracy decreased for images obtained 50–60 minutes after injection.
Intravascular contrast agents provide the opportunity for altered imaging strategies for 3D MR angiography relative to methods used for extracellular contrast agents. In this study, we explored one approach—steady-state imaging with submillimeter in-plane pixel resolution. The carotid arteries are typically imaged in less than 30 seconds by using extracellular contrast agents; with MS-325, we obtained images of the carotid arteries over 5–10 minutes by using high-spatial-resolution acquisition matrices. High-resolution images may be useful in imaging plaque ulceration, a risk factor for unstable carotid arterial plaque (21,22). A potential disadvantage of high-resolution imaging is that SNR decreases in proportion to voxel size so that additional signals acquired or improved imaging coils may be necessary to maintain adequate SNR. Also, venous enhancement may pose difficulties in image interpretation for steady-state imaging.
By using conventional targeted MIP images, 10% (three of 29) of carotid arteries were not depicted separately from the internal jugular vein on the 5-minute MS-325-enhanced images; an additional 24% (seven of 29) of vessels were somewhat obscured. Thus, in addition to altered strategies for image acquisition, altered depiction and 3D rendering algorithms are needed to take full advantage of MR angiograms with intravascular contrast agents.
For carotid arterial depiction, multiplanar reconstruction and volume-rendering methods were successfully used in this study. Volume rendering retains the 3D spatial relationships that are lost by using the MIP algorithm (13,23). This depiction method has also been useful for 3D MR angiography of the carotid arteries with extracellular contrast agents (24,25). We had good success with use of real-time volume rendering with interactive manipulation of the images by the interpreting radiologist. As an alternative, an intelligent MIP algorithm that projected only the closest vessel to the observer could be used. An additional display strategy is vessel tracking (26), in which a computer algorithm is used to find the midpoint of the vessel of interest. We also believe that the MR pulse sequence could be modified to encode the direction of flow. Phase-contrast imaging may be used, for example, to determine flow directions and velocities, which could be mapped onto the vessel of interest and separate arterial flow from venous flow by their directions in the neck. These approaches will need further evaluation in subsequent studies.
A potential role of an intravascular contrast agent is imaging multiple vascular beds after a single injection of contrast agent. Since atherosclerotic disease is a systemic process, it is useful, for example, to couple carotid MR angiography with imaging of the aortic arch (27). Our results are relevant in planning such strategies. We observed that images acquired both immediately (0-minute images) and 5–15 minutes (5-minute images) after injection were of high quality, but doses of 0.05 mmol/kg resulted in decreased accuracy compared with doses of 0.03 mmol/kg. We believe that the reduced accuracy for 0.05 mmol/kg for early images was due to background enhancement of highly vascularized tissues near the carotid artery (eg, salivary glands).
In this human study, we have now observed that steady-state images can result in substantial enhancement of background tissue, so there was actually an inverse relationship between accuracy and dose response (Table 2) for the 5-minute images. At the intermediate dose of contrast agent (0.03 mmol/kg), a 5–15-minute imaging window gave superior results compared with results with a 50–60-minute period. The MR angiographic protocol we used was optimized for the MR equipment available during the period of the study, but since readers were blinded to the doses of contrast agent, further optimization of the MR acquisition protocol, such as the flip angle, will be possible in studies in which the readers are not blinded to the doses of contrast agent. Also, higher performance gradients are now available with more efficient methods for suppression of lipids (28,29). Therefore, similar spatial resolution to that in our study is now obtained with the current generation of MR imagers in approximately 1–2 minutes or less. Finally, if a higher dose of contrast agent is necessary to prolong the imaging window, modified pulse sequences, such as inversion-recovery preparation, are also likely to be useful for background tissue suppression (30).
A major advantage of MS-325 is that similar spatial resolution should be achievable with low- and high-performance-gradient MR systems. The current approach to 3D contrast-enhanced MR angiography is to use increasingly shorter values of repetition and echo times, typically found only on advanced 1.5-T MR systems (19,31–33). Short imaging times allow separation of the carotid arterial and jugular venous phases of vascular enhancement, but this is done at the expense of spatial resolution (33). Short imaging times also allow lower doses of contrast agent, but the duration of peak arterial enhancement is extremely brief, typically a few seconds. With MS-325, short repetition and echo times are not necessary and were not used in this study. With contrast-enhanced MR angiography with extracellular contrast agents, imaging speed is frequently the overriding factor in establishing the protocol. By using MS-325 during steady-state conditions, imaging speed may no longer need to be the primary factor for MR angiographic protocol design.
There were several limitations in this study. First, the overall number of carotid arteries in each group was small, varying from eight to 24 arteries at dose groups of 0.01–0.05 mmol/kg, respectively. These numbers were further reduced because vessels in the same patient were statistically combined to reduce potential bias. The number of subjects examined will be increased in future phase III studies that are primarily designed for efficacy. Second, it would have been interesting to perform dynamic MR angiography of the carotid arteries in a manner similar to that performed with extracellular contrast agents such as gadopentetate dimeglumine. However, at the start of this study, those rapid MR angiographic pulse sequences were not widely available.
In conclusion, MS-325 has the potential to help improve spatial resolution of carotid MR angiography because of its prolonged vascular retention that results from albumin binding. For imaging 5–15 minutes after MS-325 injection, 0.03 mmol/kg appears to be an acceptable dose that maximizes CNR while minimizing soft-tissue background enhancement. At 50–60 minutes after injection of contrast agent, the overall image quality decreases, so that a shorter imaging window (eg, up to 30 minutes after injection of contrast agent) could be explored in the future. Finally, because of nonselective venous and arterial enhancement, alternate image acquisition or display strategies such as volume rendering will need to be implemented to prevent carotid arterial signal intensity from being obscured by internal jugular venous signal intensity.
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ACKNOWLEDGMENTS |
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FOOTNOTES |
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Author contributions: Guarantors of integrity of entire study, D.A.B., E.K.Y.; study concepts, D.A.B., E.K.Y.; study design, T.M.G., J.A.P., E.K.Y.; literature research, D.A.B.; clinical studies, D.A.B., A.E.S., K.G.B., T.M.G., R.A.B., R.D., E.S.M.; data acquisition, D.A.B., A.E.S., K.G.B., T.M.G., R.A.B., R.D., E.S.M.; data analysis/interpretation, all authors; statistical analysis, D.A.B., J.A.P., E.K.Y.; manuscript preparation and definition of intellectual content, D.A.B., E.K.Y.; manuscript editing, D.A.B.; manuscript revision/review, D.A.B., E.K.Y.; manuscript final version approval, D.A.B.
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REFERENCES |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTS DISCUSSIONREFERENCES |
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